Evaluation of aerodigestive disease and diagnosis of sliding hiatal hernia in brachycephalic and nonbrachycephalic dogs

Abstract Background Aerodigestive diseases (AeroD), hybrid disorders between the respiratory and gastrointestinal (GI) tracts, may present without GI signs. Sliding hiatal hernia (sHH) is an important AeroD in brachycephalic dogs linked to respiratory pathology. The spectrum of other AeroD and respiratory clinical signs (CS) in brachycephalic and nonbrachycephalic dogs with sHH is unknown. Objectives Characterize CS of AeroD in dogs with sHH, compare CS between brachycephalic and nonbrachycephalic dogs, and compare thoracic radiographs and videofluoroscopic swallow study (VFSS) for diagnosing sHH. Animals Sixty‐seven client‐owned dogs with sHH. Methods Medical records of dogs with sHH presented to the veterinary teaching hospitals at Auburn University and the University of Missouri between 1 January 2009 and 31 December 2020 were retrospectively reviewed. Between group, comparisons were made using Mann‐Whitney test, Chi‐square analysis, and Spearman correlation (P < .05). Results Dogs with sHH presented with exclusively GI signs (28/67), mixed respiratory and GI signs (22/67), or with exclusively respiratory signs (17/67). Wheras brachycephalic dogs were not significantly more likely to present with respiratory CS (P = .145), they were younger (P < .001), and more likely to present in respiratory distress (P = .02), and with radiographic evidence of aspiration pneumonia (P < .001) compared to nonbrachycephalic dogs. Six of 12 dogs with normal thoracic radiographs having sHH presented with respiratory CS. For detection of sHH, VFSS was superior to radiographs (P < .001). Conclusions and Clinical Importance Dogs with sHH may present with exclusively respiratory signs. Respiratory signs may be more severe in brachycephalic compared to nonbrachycephalic dogs. Videofluoroscopic swallow study was superior to thoracic radiographs for detection of sHH in dogs.


| INTRODUCTION
Aerodigestive diseases (AeroD) are important hybrid disorders between the respiratory and gastrointestinal (GI) tracts and reflect complex, coordinated events required for breathing and swallowing. Aerodigestive diseases are known contributors to respiratory clinical signs in both people and dogs. Some examples of AeroD include brachycephalic obstructive airway syndrome, aspiration pneumonia and aspiration pneumonitis, diffuse aspiration bronchiolitis, gastroesophageal reflux disease (GERD), and extraesophageal reflux disease (EERD, defined as refluxate extending beyond the esophagus to contact structures of the upper airway causing pathology). [1][2][3][4][5][6][7][8] Importantly, AeroD may present in the absence of GI clinical signs (CS) and with normal thoracic radiographs making clinical recognition challenging. 2 Correction of the underlying AeroD has been demonstrated to improve clinical outcome, making identification of AeroD critical for optimal case management. 6,[9][10][11] Sliding hiatal hernias (sHH; hiatal hernia type 1) are known contributors to GI CS in dogs that have been linked to GERD, EERD, and respiratory pathology, making them an example of an AeroD. 2 Sliding hiatal hernias frequently are identified in brachycephalic dogs, with breed predispositions in French bulldogs 12 and Chinese Shar Peis. 13 However, sHH is not exclusive to this population. Gastroesophageal reflux disease is closely associated with sHH in people, with compromised esophageal clearance, increased transient lower esophageal sphincter relaxation, and gastroesophageal junction incompetence contributing to both typical and atypical GERD clinical signs, as well as several other aspiration-associated respiratory syndromes (AARS). [14][15][16] Brachycephalic dogs are considered to be at increased risk for GERD and AARS because of upper airway obstruction. 9 An association between GERD and sHH has been identified in brachycephalic, but not nonbrachycephalic dogs with sHH. 17,18 The presenting CS and classification of concurrent AeroD, such as GERD, in brachycephalic compared to nonbrachycephalic dogs with sHH are unknown.
Thoracic radiographs historically have been used to detect sHH in dogs. 19 However, conventional radiography may be poorly sensitive for the detection of sHH and accompanying episodic or dynamic AeroD, including reflux. [20][21][22] Videofluoroscopic swallow studies (VFSS) represent the criterion standard for evaluation of dysphagia in veterinary medicine and may be superior for detecting and characterizing sHH and accompanying AeroD in dogs. 23 Our primary objectives were 3-fold. The first aim was to characterize CS of AeroD in dogs with sHH. The second aim was to compare clinical and demographic features between brachycephalic and nonbrachycephalic dogs with sHH, and the final aim was to compare thoracic radiographs and VFSS for diagnosing sHH. We hypothesized that in dogs with sHH respiratory CS would be common and associated with pathologic reflux, with CS more common and severe and pathologic reflux more frequent in brachycephalic dogs versus nonbrachycephalic dogs. We also hypothesized that VFSS would be superior to radiographs for diagnosing sHH.  24 In all cases, VFSS were standing and free-feeding studies as previously described. 23  Comparisons between VFSS and radiographs for detecting sHH were performed on a subpopulation of dogs that was evaluated by both modalities. A P < .05 significance level was assigned in all cases.

| Animals
Sixty-seven client-owned companion dogs met inclusion criteria: MU-VHC (n = 52), AU-CVM (n = 15). Twenty-three breeds were represented ( Repetitive "dry" swallowing b 0 1 1 Note: Clinical signs were included in the study where there was a change in severity noted in the medical record prompting veterinary medical evaluation. Dogs may have had >1 respiratory or GI CS. a Dogs requiring emergency intervention at the time of presentation were considered to be in in respiratory distress whereas labored breathing referred to dogs that increased respiratory effort but did not require emergency stabilization. b A "dry" swallow refers to spontaneous, reflexive swallowing that occurs without eating or drinking. *Statistically significant comparisons (P < .05). a combination of respiratory and GI CS (n = 22), or exclusively for respiratory CS (n = 17). Reported respiratory and GI CS are provided in Table 2. Median (IQR) duration of CS was 3 months (1-7.3 months; range, 1 day-5 years).  Table 3. Six of 12 dogs with normal thoracic radiographs presented for respiratory or mixed respiratory and GI clinical signs.

| Diagnostic imaging
A sHH was diagnosed by thoracic radiographs in 36/66 (55%) dogs and by VFSS in 36/38 (95%) dogs. Of 37 dogs that had both thoracic radiographs and VFSS, the sHH was identified by both modalities in 6. A sHH was diagnosed incidentally during an exploratory laparotomy in 1 dog presented for vomiting. This dog was evaluated by both thoracic radiographs and VFSS. For dogs having both radiographs and VFSS (n = 37), diagnosis of sHH was made significantly more often with VFSS (P < 0.001). A summary is provided in Table 4.
Reflux margination was as follows: EER (n = 4), proximal esophagus (n = 14), middle esophagus (n = 9), and distal (n = 5). As such, 27 and   The second dog underwent a thoracic CT after developing a pneumothorax after surgical correction of the sHH. Atelectasis or fibrosis associated with the right middle lung lobe was identified in this dog.

| Final diagnoses
Diagnoses of concurrent aeroD and other respiratory or digestive disorders not currently classified as aeroD are provided in Table 4.  30 Although respiratory CS have been reported in dogs with sHH, they were in brachycephalic breeds and consistent with BOAS. 30 The high incidence of respiratory CS in 58% of dogs in our study is consistent with a recent report finding that dogs presenting with respiratory CS frequently have occult alimentary disease. 2 In our study, 25% of dogs were presented with exclusively respiratory CS. As such, reliance on GI CS to identify patients with sHH is likely to be poorly sensitive. Maintaining an index of suspicion of sHH as an AeroD presenting in the absence of GI CS may improve identification by prompting additional diagnostic testing.

T A B L E 5 Summary of recognized aerodigestive diseases in dogs with sliding hiatal hernia
Normal thoracic radiographs were identified in 12 dogs with sHH, including 6 that were presented with CS of respiratory disease. The lack of radiographic findings in this group may be a consequence of the relatively poor sensitivity of thoracic radiographs to detect subtle disease. In people however extrathoracic cough triggers including irritation by acid and pepsin on the larynx and pharynx, microaspiration, and cough sensitization secondary to GERD and EERD are likely contributors to respiratory CS in the absence of overt radiographic abnormalities. 31 Cough sensitization refers to a condition in which the cough reflex is more readily induced, and has been linked to GERD and nasal disease in people. 32 Of interest, fluid in the esophagus noted on thoracic radiography (interpreted as of unknown clinical relevance) was associated with pathologic reflux in 6/7 dogs that subsequently underwent VFSS. Follow-up evaluation by VFSS in dogs with radiographic evidence of esophageal fluid and supportive CS thus may be indicated. After sHH, AP was the most commonly identified abnormality on thoracic radiographs. However, AP, particularly when recurrent, should be considered an indication of failed airway protection and warrants additional diagnostic testing to identify a predisposing cause.
Historically, thoracic radiography is used to diagnose sHH as well as underlying respiratory disease. However, in dynamic disease processes such as sHH, GERD, and EERD, conventional radiographs are likely to be poorly sensitive. Videofluoroscopic swallow studies represent the criterion standard for evaluation of dysphagia in dogs. 2,23 In our study, VFSS was superior to radiographs for detecting sHH. Furthermore, this modality allowed characterization of concurrent AeroD such as GERD. In our study, 84% (32/38) of dogs with sHH were found to have detectable reflux on swallow. Furthermore, VFSS allowed discrimination between physiologic and pathologic reflux based on the degree of margination. This differentiation is not possible by thoracic radiographs. However, VFSS lack the resolution to detect pulmonary parenchymal and airway-related changes compared to thoracic radiographs. As such, a multimodal approach encompassing both VFSS and conventional respiratory imaging is warranted when evaluating dogs suspected of having sHH. 33,34 The presence of concurrent AeroD such as GERD and EERD is supported by previous studies in both dogs and people. 17 and in a study that identified reflux in 88% of dogs with sHH. 17 However, the degree of margination was not evaluated. The frequency of pathologic reflux in this population may be attributed in part to loss of extrinsic pressures from the diaphragmatic crura and cranial displacement of the esophageal gastric junction. 36 However, incomplete resolution of GERD after successful surgery for sHH in a previous study may suggest that GERD is an independent or multifactorial process occurring in combination with sHH, and treatment for reflux may be required after surgery. 17 In our study, several concurrent conditions that increase upper airway resistance were identified. In 22/34 brachycephalic dogs, BOAS was considered severe enough to warrant surgical correction.
Although less common, upper airway obstruction also was identified in nonbrachycephalic dogs, including laryngeal paralysis (n = 2), grade 2 laryngeal collapse (n = 1) tracheal collapse (n = 2), mainstem bronchial collapse (n = 2), and a nasal mass (n = 1 Prospective studies comparing VFSS and radiographs for detecting sHH are warranted. Additionally, the influence of BOAS on the severity of respiratory clinical signs in the patient population cannot be entirely predicted. However, we attempted to mitigate this situation by not including CS for analysis unless they were listed as progressive or the reason for seeking veterinary medical attention. In dogs in which a concurrent respiratory disease was identified (eg, chronic bronchitis) the contribution of sHH, reflux, and microaspiration on airway inflammation could not be determined and thus it was unclear if these diseases represented an AeroD or were a comorbid condition.

| CONCLUSION
The use of VFSS to screen patients for sHH improves detection and provides more comprehensive evaluation of concurrent AeroD compared to thoracic radiographs alone. Nonbrachycephalic dogs with sHH were commonly identified in our study. However, brachycephalic dogs presented at a younger age and with more evidence severe respiratory compromise compared to nonbrachycephalic dogs. Sliding hiatal hernias are important AeroD in dogs with the potential to cause severe CS, including those exclusive to the respiratory tract. As such, clinical awareness of the relationship between the respiratory and GI tracts is needed to maximize the identification of diseases in affected patients.

ACKNOWLEDGMENT
No funding was received for this study.